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Cadmium toxicity to Microcystis aeruginosa PCC 7806 and its microcystin-lacking mutant.

Huang B, Xu S, Miao AJ, Xiao L, Yang LY - PLoS ONE (2015)

Bottom Line: The adverse effects of microcystin (MC) produced by cyanobacteria have drawn considerable attention from the public.Yet it remains unclear whether MC confers any benefits to the cyanobacteria themselves.Although the inactivation of MC peptide synthetase gene had some nutrient and Cd concentration dependent effects on the parameters above, both cyanobacterial strains showed the same Cd accumulation ability and displayed similar Cd sensitivity.

View Article: PubMed Central - PubMed

Affiliation: State Key Laboratory of Pollution Control and Resource Reuse, School of the Environment, Nanjing University, Nanjing, Jiangsu Province, China.

ABSTRACT
The adverse effects of microcystin (MC) produced by cyanobacteria have drawn considerable attention from the public. Yet it remains unclear whether MC confers any benefits to the cyanobacteria themselves. One suggested function of MC is complexation, which may influence the bioaccumulation and toxicity of trace metals. To test this hypothesis, we examined Cd toxicity to wild-type Microcystis aeruginosa PCC 7806 (WT) and its MC-lacking mutant (MT) under nutrient-enriched (+NP), phosphorus-limited (-P), and nitrogen-limited (-N) conditions. The accumulation of Cd and the biochemical parameters associated with its detoxification [total phosphorus (TP), inorganic polyphosphate (Poly-P), and glutathione (GSH) in the cells as well as intra- and extra-cellular carbohydrates] were quantified. Although the -P cyanobacteria accumulated less Cd than their +NP and -N counterparts, the different nutrient-conditioned cyanobacteria were similarly inhibited by similar free ion concentration of Cd in the medium ([Cd2+]F). Such good toxicity predictability of [Cd2+]F was ascribed to the synchronous decrease in the intracellular concentrations of Cd and TP. Nevertheless, Cd toxicity was still determined by the intracellular Cd to phosphorus ratio (Cd/P), in accordance with what has been reported in the literature. On the other hand, the concentrations of TP, Poly-P, and carbohydrates went up, but GSH concentration dropped down with the enhancement of [Cd2+]F, indicating their association with Cd detoxification. Although the inactivation of MC peptide synthetase gene had some nutrient and Cd concentration dependent effects on the parameters above, both cyanobacterial strains showed the same Cd accumulation ability and displayed similar Cd sensitivity. These results suggest that MC cannot affect metal toxicity either by regulating metal accumulation or by altering the detoxification ability of the cyanobacteria. Other possible functions of MC need to be further investigated.

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Cell-volume-normalized concentration of (a, d, g) monosaccharide and (b, e, h) polysaccharide excreted by the cells as well as (c, f, i) cellular concentration of carbohydrates retained inside the cells in the (a-c) nutrient-enriched (+NP), (d-f) phosphorus-limited (-P), and (g-i) nitrogen-limited (-N) toxicity tests for Microcystis aeruginosa PCC 7806 (WT, black bar) and its MC-lacking mutant (MT, white bar).All values were normalized to levels (100% as represented by the dashed lines) detected in the WT strain at the lowest respective Cd concentration (Treatment A). Cd concentration in treatments A-H ([Cd]T, 1.00×10-8—9.95×10-6 M; [Cd2+]F, 1.00×10-13—1.21×10-8 M) is listed in Table B of S1 File. Data are mean ± standard error (n = 2)
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pone.0116659.g004: Cell-volume-normalized concentration of (a, d, g) monosaccharide and (b, e, h) polysaccharide excreted by the cells as well as (c, f, i) cellular concentration of carbohydrates retained inside the cells in the (a-c) nutrient-enriched (+NP), (d-f) phosphorus-limited (-P), and (g-i) nitrogen-limited (-N) toxicity tests for Microcystis aeruginosa PCC 7806 (WT, black bar) and its MC-lacking mutant (MT, white bar).All values were normalized to levels (100% as represented by the dashed lines) detected in the WT strain at the lowest respective Cd concentration (Treatment A). Cd concentration in treatments A-H ([Cd]T, 1.00×10-8—9.95×10-6 M; [Cd2+]F, 1.00×10-13—1.21×10-8 M) is listed in Table B of S1 File. Data are mean ± standard error (n = 2)

Mentions: Being the major component of exopolymeric substances, carbohydrates play an important role in metal biogeochemical cycling and detoxification [47]. In the present study, Cd not only induced the synthesis or slowed the degradation of carbohydrates in M. aeruginosa cells but also accelerated their excretion into the experimental medium (Fig. 4 and Figure B in S1 File). In the +NP toxicity test for WT, there was 1.23, 0.99, and 1.45 time significant (p < 0.05, one-way ANOVA) enhancement in [CHO]mono, [CHO]poly, and [CHO]cell, respectively, when [Cd2+]F went up from 1×10-13 M in the control treatment to 1×10-9 M in treatment H. Up-regulated production of extracellular polysaccharides was previously found to be a general response to Cu, Cd, and Ag in various marine phytoplankton [23, 37]. Moreover, the polysaccharides of the cyanobacterium Anabaena spiroides have a high binding affinity to Mn, Cu, Pb, and Hg [48]. In particular, alginic acid as a typical polysaccharide is able to reduce metal accumulation by the American oyster (Crassostrea virginica) [49]. These findings suggest that carbohydrates could mitigate metal toxicity through chelation. Nevertheless, other possibilities like the relief of metal-induced oxidative stresses by carbohydrates cannot be excluded [50]. Based on the results of two-way ANOVA (Table C in S1 File), [CHO]mono, [CHO]poly, and [CHO]cell displayed significant (p < 0.05) difference between WT and MT. However, no consistent trend was found either for the different nutrient-conditioned M. aeruginosa or for the same nutrient-conditioned cells at different [Cd2+]F. This phenomenon implies strong interactions between MC, nutrient limitation, and ambient Cd concentration, which need to be further investigated.


Cadmium toxicity to Microcystis aeruginosa PCC 7806 and its microcystin-lacking mutant.

Huang B, Xu S, Miao AJ, Xiao L, Yang LY - PLoS ONE (2015)

Cell-volume-normalized concentration of (a, d, g) monosaccharide and (b, e, h) polysaccharide excreted by the cells as well as (c, f, i) cellular concentration of carbohydrates retained inside the cells in the (a-c) nutrient-enriched (+NP), (d-f) phosphorus-limited (-P), and (g-i) nitrogen-limited (-N) toxicity tests for Microcystis aeruginosa PCC 7806 (WT, black bar) and its MC-lacking mutant (MT, white bar).All values were normalized to levels (100% as represented by the dashed lines) detected in the WT strain at the lowest respective Cd concentration (Treatment A). Cd concentration in treatments A-H ([Cd]T, 1.00×10-8—9.95×10-6 M; [Cd2+]F, 1.00×10-13—1.21×10-8 M) is listed in Table B of S1 File. Data are mean ± standard error (n = 2)
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4295860&req=5

pone.0116659.g004: Cell-volume-normalized concentration of (a, d, g) monosaccharide and (b, e, h) polysaccharide excreted by the cells as well as (c, f, i) cellular concentration of carbohydrates retained inside the cells in the (a-c) nutrient-enriched (+NP), (d-f) phosphorus-limited (-P), and (g-i) nitrogen-limited (-N) toxicity tests for Microcystis aeruginosa PCC 7806 (WT, black bar) and its MC-lacking mutant (MT, white bar).All values were normalized to levels (100% as represented by the dashed lines) detected in the WT strain at the lowest respective Cd concentration (Treatment A). Cd concentration in treatments A-H ([Cd]T, 1.00×10-8—9.95×10-6 M; [Cd2+]F, 1.00×10-13—1.21×10-8 M) is listed in Table B of S1 File. Data are mean ± standard error (n = 2)
Mentions: Being the major component of exopolymeric substances, carbohydrates play an important role in metal biogeochemical cycling and detoxification [47]. In the present study, Cd not only induced the synthesis or slowed the degradation of carbohydrates in M. aeruginosa cells but also accelerated their excretion into the experimental medium (Fig. 4 and Figure B in S1 File). In the +NP toxicity test for WT, there was 1.23, 0.99, and 1.45 time significant (p < 0.05, one-way ANOVA) enhancement in [CHO]mono, [CHO]poly, and [CHO]cell, respectively, when [Cd2+]F went up from 1×10-13 M in the control treatment to 1×10-9 M in treatment H. Up-regulated production of extracellular polysaccharides was previously found to be a general response to Cu, Cd, and Ag in various marine phytoplankton [23, 37]. Moreover, the polysaccharides of the cyanobacterium Anabaena spiroides have a high binding affinity to Mn, Cu, Pb, and Hg [48]. In particular, alginic acid as a typical polysaccharide is able to reduce metal accumulation by the American oyster (Crassostrea virginica) [49]. These findings suggest that carbohydrates could mitigate metal toxicity through chelation. Nevertheless, other possibilities like the relief of metal-induced oxidative stresses by carbohydrates cannot be excluded [50]. Based on the results of two-way ANOVA (Table C in S1 File), [CHO]mono, [CHO]poly, and [CHO]cell displayed significant (p < 0.05) difference between WT and MT. However, no consistent trend was found either for the different nutrient-conditioned M. aeruginosa or for the same nutrient-conditioned cells at different [Cd2+]F. This phenomenon implies strong interactions between MC, nutrient limitation, and ambient Cd concentration, which need to be further investigated.

Bottom Line: The adverse effects of microcystin (MC) produced by cyanobacteria have drawn considerable attention from the public.Yet it remains unclear whether MC confers any benefits to the cyanobacteria themselves.Although the inactivation of MC peptide synthetase gene had some nutrient and Cd concentration dependent effects on the parameters above, both cyanobacterial strains showed the same Cd accumulation ability and displayed similar Cd sensitivity.

View Article: PubMed Central - PubMed

Affiliation: State Key Laboratory of Pollution Control and Resource Reuse, School of the Environment, Nanjing University, Nanjing, Jiangsu Province, China.

ABSTRACT
The adverse effects of microcystin (MC) produced by cyanobacteria have drawn considerable attention from the public. Yet it remains unclear whether MC confers any benefits to the cyanobacteria themselves. One suggested function of MC is complexation, which may influence the bioaccumulation and toxicity of trace metals. To test this hypothesis, we examined Cd toxicity to wild-type Microcystis aeruginosa PCC 7806 (WT) and its MC-lacking mutant (MT) under nutrient-enriched (+NP), phosphorus-limited (-P), and nitrogen-limited (-N) conditions. The accumulation of Cd and the biochemical parameters associated with its detoxification [total phosphorus (TP), inorganic polyphosphate (Poly-P), and glutathione (GSH) in the cells as well as intra- and extra-cellular carbohydrates] were quantified. Although the -P cyanobacteria accumulated less Cd than their +NP and -N counterparts, the different nutrient-conditioned cyanobacteria were similarly inhibited by similar free ion concentration of Cd in the medium ([Cd2+]F). Such good toxicity predictability of [Cd2+]F was ascribed to the synchronous decrease in the intracellular concentrations of Cd and TP. Nevertheless, Cd toxicity was still determined by the intracellular Cd to phosphorus ratio (Cd/P), in accordance with what has been reported in the literature. On the other hand, the concentrations of TP, Poly-P, and carbohydrates went up, but GSH concentration dropped down with the enhancement of [Cd2+]F, indicating their association with Cd detoxification. Although the inactivation of MC peptide synthetase gene had some nutrient and Cd concentration dependent effects on the parameters above, both cyanobacterial strains showed the same Cd accumulation ability and displayed similar Cd sensitivity. These results suggest that MC cannot affect metal toxicity either by regulating metal accumulation or by altering the detoxification ability of the cyanobacteria. Other possible functions of MC need to be further investigated.

Show MeSH
Related in: MedlinePlus